Commonalities in Segmentation Processes: Are There Any?
I will end with a similar question to the one I started with: What—if anything—do diverse segmentation processes have in common? A detailed comparison reveals that in fact, there is very little in common, and almost no generalizations one can make about segmentation as a developmental process. This is in contrast with segments as morphological units, w'hich while probably convergent, do have enough in common to justify being discussed together. Nonetheless, there are numerous restricted developmental commonalities, found in specific taxa. The phylogenetic distribution of these commonalities in different aspects of the process allows a reconstruction of the evolutionary history of segmentation, both as a developmental and as a morphological phenomenon. This makes it possible to identify specific nodes in animal phylog- eny where there were significant changes in development that led to segments in the first place (Chipman, 2019) and nodes where there were changes in the development of segments once they had evolved (Balavoine, 2014; Stahi and Chipman, 2016). Coupled with information from the fossil record, and with data about morphology and life history, we can begin to reconstruct the success story of segmented animals and to understand how and why they evolved.
Alwes, F., B. Hinchen, and C. G. Extavour. 2011. Patterns of cell lineage, movement, and migration from germ layer specification to gastrulation in the amphipod crustacean Parhyale hawaiensis. Dev. Biol. 359: 110-123.
Aulehla, A., and B. G. Herrmann. 2004. Segmentation in vertebrates: Clock and gradient finally joined. Genes Dev. 18: 2060-2067.
Auman, T., and A. D. Chipman. 2018. Growth zone segmentation in the milkweed bug Oncopeltus fasciatus sheds light on the evolution of insect segmentation. BMC Evol. Biol. 18: 178.
Auman. T.. В. M. I. Vreede. A. Weiss, S. D. Hester, T. A. Williams, L. M. Nagy, and A. D. Chipman. 2017. Dynamics of growth zone patterning in the milkweed bug Oncopeltus fasciatus. Development 144: 1896-1905.
Balavoine, G. 2014. Segment formation in Annelids: Patterns, processes and evolution. Int. J. Dev. Biol. 58: 469-483.
Bely, A. E., E. E. Zattara, and J. M. Sikes. 2014. Regeneration in spiralians: Evolutionary patterns and developmental processes. Int. J. Dev. Biol. 58: 623-634.
Bleidorn, С., C. Helm, A. Weigert, and M. T. Aguado. 2015. Annelida. In Evolutionary Developmental Biology of Invertebrates, Vol. 2, Ed. A. Wanninger, 193-230. Wien: Springer-Verlag.
Chipman, A. D. 2010. Parallel evolution of segmentation by co-option of ancestral gene regulatory networks. Bioessays 32: 60-70.
Chipman, A. D. 2015. An embryological perspective on the early arthropod fossil record. BMC Evol. Biol. 15: 285.
Chipman, A. D. 2019. Becoming segmented. In Perspectives on Evolutionary Developmental Biology, Ed. G. Fusco, 235-244. Padova: Padova University Press.
Chipman, A. D., and M. Akam. 2008. The segmentation cascade in the centipede Strigamia maritima: Involvement of the Notch pathway and pair-rule gene homologues. Dev. Biol. 319: 160-169.
Chipman, A. D., W. Arthur, and M. Akam. 2004. Early development and segment formation in the centipede Strigamia maritima (Geophilomorpha). Evol. Dev. 6: 78-89.
Choe, С. P, S. C. Miller, and S. J. Browm. 2006. A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. Proc. Natl. Acad. Sci. USA 103: 6560-6564.
Cooke, J., and E. C. Zeeman. 1976. Clock and w'avefront model for control of number of repeated structures during animal morphogenesis. J. Theoret. Biol. 58: 455-476.
Dohle, W., and G. Scholtz. 1988. Clonal analysis of the crustacean segment - The discordance between genealogical and segmental borders. Development 104: 147-160.
Dubrulle, J., and O. Pourquie. 2004. Coupling segmentation to axis formation. Development 131: 5783-5793.
Fischer, A. H. L., T. Henrich, and D. Arendt. 2010. The normal development of Platynereis dumerilii (Nereididae, Annelida). Front. Zool. 7: 31.
Fu, D., J. Ortega-Hernandez, A. C. Daley, X. Zhang, and D. Shu. 2018. Anamorphic development and extended parental care in a 520 million-year-old stem-group euarthropod from China. BMC Evol. Biol. 18: 147.
Gerberding, M., W. E. Browne, and N. H. Patel. 2002. Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129: 5789-5801.'
Gerberding, M., and G. Scholtz. 1999. Cell lineage of the midline cells in the amphipod crustacean Orchestia cavimana (Crustacea, Malacostraca) during formation and separation of the germ band. Dev. Genes Evol. 209: 91-102.
Hannibal, R. L„ and N. H. Patel. 2013. What is a segment? Evodevo 4: 35.
Hannibal, R. L., A. L. Price, and N. H. Patel. 2012. The functional relationship between ectodermal and mesodermal segmentation the crustacean, Parhyale hawaiensis. Dev. Biol. 361: 427-438.
Hartenstein, V., and A. D. Chipman. 2015. Hexapoda: A Drosophila’s view of insect development. In Evolutionary Developmental Biology of Invertebrates, Vol. 5, Ed. A. Wanninger, 1-91. Vienna: Springer.
Hopkins, M. 2017. Development, trait evolution, and the evolution of development in trilo- bites. Ini. Comp. Biol. 57: 488-498.
Hughes, N. C., A. Minelli, and G. Fusco. 2006. The ontogeny of trilobite segmentation: A comparative approach. Paleobiology 32: 602-627.
Janssen, R., G. E. Budd, and W. G. M. Damen. 2011. Gene expression suggests conserved mechanisms patterning the heads of insects and myriapods. Dev. Biol. 357: 64-72.
Kuo, D. H., and M. Shankland. 2004. A distinct patterning mechanism of О and P cell fates in the development of the rostral segments of the leech Helobdella robusta: Implications for the evolutionary dissociation of developmental pathway and morphological outcome. Development 131: 105-115.
Lans, D., C. J. Wedeen, and D. A. Weisblat. 1993. Cell lineage analysis of the expression of an engrailed homolog in leech embryos. Development 117: 857-871.
Minelli, A. 2001. A three-phase model of arthropod segmentation. Dev. Genes Evol. 211: 509-521.
Minelli, A., and G. Fusco. 2004. Evo-devo perspectives on segmentation: Model organisms, and beyond. Trends Ecol. Evol. 19: 423-429.
Nakamoto, A., S. D. Hester, S. J. Constantinou, W. G. Blaine, A. B. Tewksbury, M. T. Matei, ..., T. A. Williams. 2015. Changing cell behaviours during beetle embryogen- esis correlates with slowing of segmentation. Nat. Commun. 6: 6635.
Palmeirim, I., D. Henrique, D. Ish-Horowicz, and O. Pourquie. 1997. Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somito- genesis. Cell 91: 639-648.
Posnien, N„ J. B. Schinko, S. Kittelmann, and G. Bucher. 2010. Genetics, development and composition of the insect head - A beetle’s view. Arthropod Struct. Dev. 39: 399-410.
Pourquie, O. 2003. The segmentation clock: Converting embryonic time into spatial pattern. Science 301: 328-330.
Scholtz, G. 2002. The Articulata hypothesis - or what is a segment? Org. Divers. Evol. 2: 197-215.
Scholtz, G., and G. D. Edgecombe. 2006. The evolution of arthropod heads: Reconciling morphological, developmental and palaeontological evidence. Dev. Genes Evol. 216: 395-415.
Scholtz, G„ and C. Wolff. 2002. Cleavage, gastrulation, and germ disc formation of the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Contrib. Zool. 71:9-28.
Schoppmeier, M., and W. G. M. Damen. 2005a. Expression of Pax group III genes suggests a single-segmental periodicity for opisthosomal segment patterning in the spider Cupiennius salei. Evol. Dev. 7: 160-169.
Schoppmeier, M., and W. G. M. Damen. 2005b. Suppressor of hairless and Presenilin phenotypes imply involvement of canonical Notch-signalling in segmentation of the spider Cupiennius salei. Dev. Biol. 280: 211-224.
Stahi, R., and A. D. Chipman. 2016. Blastoderm segmentation in Oncopeltus fascialus and the evolution of arthropod segmentation mechanisms. Proc. R. Soc. Lond. В 283: 20161745.
Stollewerk, A., M. Schoppmeier, and W. G. M. Damen. 2003. Involvement of Notch and Delta genes in spider segmentation. Nature 423: 863-865.
Williams, T. A., and L. M. Nagy. 2017. Linking gene regulation to cell behaviors in the posterior growth zone of sequentially segmenting arthropods. Arthropod Struct. Dev. 46: 380-394.
Wolfe, J. M. 2017. Metamorphosis is ancestral for crown euarthropods, and evolved in the Cambrian or earlier. Integr. Comp. Biol. 57: 499-509.
Wolff, C., and G. Scholtz. 2002. Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev. Biol. 250: 44-58.
Zattara, E. E. and A. E. Bely. 2016. Phylogenetic distribution of regeneration and asexual reproduction in Annelida: Regeneration is ancestral and fission evolves in regenerative clades. Invertehr. Biol. 135: 400-414.